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109
On the Functional Morphology of the Alimentary Tract

of Some Fish in Relation to Differences in their Feeding
Habits: Anatomy and Histology
BY
A. H. AL-HUSSAINI, M.Sc. (Cairo), P H . D . (Sheffield)
(From the Department of Zoology, The University of Sheffield)
With Three Plates
CONTENTS
PACE
INTRODUCTION . . . . . . . . . . . . . 109
HISTORICAL SURVEY . . . . . . . . . . . . 1 1 0
M A T E R I A L A N DM E T H O D S . . 1 1 1
A N A T O M Y O F T H EA L I M E N T A R Y T R A C T . . . . . . . . . 1 1 1
T h e Protractile Apparatus of t h e M o u t h . . . . . . . . 1 1 1
T h e Pharyngeal Dental Apparatus . . . . . . . . . 113
T h e Mechanism of Deglutition . . . . . . . . - U S
T h e Intestinal T u b e 117
T h e Mucosal Folds . . . . . . . . . . . 1 1 9
T h e Surface Area of t h e Intestinal M u c o s a . . . . . . . 1 2 0
H I S T O L O G Y O F T H EA L I M E N T A R Y T R A C T . . . . . . . - 1 2 3
T h e Buccal Cavity. . . . . . . . . . . . 124
The Pharynx 127
T h e Anterior Pharynx . . . . . . . . . - 1 2 7
T h e Posterior Pharynx 128
T h e Oesophagus . . . . . . . . . . . . 129
T h e Intestine . . . . . . . . . . . - 1 3 1
DISCUSSION 134
ACKNOWLEDGEMENTS 136
SUMMARY 136
REFERENCES . . . . . . . . . . . . 137
EXPLANATION OF PLATES . . . . . . . . . . . 1 3 8
L I S T O F ABBREVIATIONS USED I N T H EILLUSTRATIONS . . . . . - 1 3 9
INTRODUCTION
HE present work is the continuation of a series of studies (Al-Hussaini,
T 1945-7) attempting to correlate the structure of the alimentary canal
with the feeding habits of teleosts. These earlier studies were based on dis-
tantly related species and thus the differences observed and described might
well be due to congenital factors rather than to purely adaptive causes—of this
no certain answer can yet be given. The present study is an attempt to exclude
congenital factors as nearly as possible by choosing three closely allied species
[Quarterly Journal Microscopical Science, Vol. 90, part 2, June 1949]
2421.10 T
no Al-Hussaini—Functional Morphology of the Alimentary
with different feeding habits, namely, the mirror (king or Spiegel) carp
(Cyprinus carpio L.), the roach (Rutilus rutilus (L.)), and the gudgeon (Gobio
gnbio (L.)), species which will hereafter be referred to by their generic names
only. From the point of view of the general problem this series suffers from a
slight defect in that all three are capable of dealing with a mixed diet, that is,
they are strictly speaking omnivorous. Nevertheless, the mirror carp (similar
in feeding habits to the common carp) ingests more plant than animal food
(Couch, 1865; Day, 1880-4; Regan, 1911), in the gudgeon animal food pre-
ponderates in the diet (Yarrell, 1841; Day, 1880-4; Susta, 1888; Regan, 1911,
Hartley, 1940, 1947), while the roach is omnivorous in the true sense (Greve,
1897; Regan. 1911; Hartley, 1940, 1947), and they have been customarily
described as herbivorous, carnivorous, and omnivorous feeders according to
the material which composes the greater bulk of their diet. An attempt was
made to justify these conclusions experimentally, but unfortunately, owing
to unavoidable circumstances, the number of fish which could eventually be
spared was very small, so that not more than some three or four individuals
could be fed on any one specialized diet. Such results as were obtained,
however, supported the view above expressed. It may be noted further that
the carp and the gudgeon both seek their food from the bottom.
The present account deals simply with the comparative anatomy and his-
tology of the mouth, pharynx, and gut of the three types. This will be followed
by an account of the cytological, lustochemical, and physiological aspects of
the problem so that the 'functional morphology' and the adaptive correlations
may thereby acquire a firmer basis.
HISTORICAL SURVEY
Good historical reviews of early work have been written by Oppel (1896),
Sullivan (1907), and Biedermann (1911), and it is not proposed to add much
to them beyond what is necessary to provide an appropriate background for
the present study. Amongst the more important works that have appeared
since these reviews may be mentioned Jacobshagen (1911, 1913, 1915, 1937).
who extended Eggeling's (1907) earlier study of the detailed configuration of
the intestinal mucosa, from both taxonomic and adaptive points of view,
while Pictet (1909) working on similar lines studied, in particular, the gut
mucosa of five Cyprinid species. Dawes (1929) described the histology of the
gut of the plaice and defined the pharynx, oesophagus, and rectum, pointing
out certain changes in hoth cytoplasm and nucleus of the columnar epithelial
cells which he associated with secretory activity. Of the more recent workers
directly concerned with Cyprinids, mention must be made of Rogick (1931)
working on Campostoma anomalum, and of Curry (1939) who studied the
common carp—Cyprinus carpio communis. Sarbahi (1940) differentiated a
caeca! from a pyloric portion of the intestinal bulb and described conical
cells which hang freely into the lumen of the rectum in Labeo rohita. McVay
and Kaan (1940) investigated the goldfish—Carassius auratus—and discerned
the changes which occur in the cells of the intestinal epithelium, already
Tract of Some Fish in Relation to their Feeding Habits 111
referred to by Dawes, but offered no explanation of the phenomenon. Finally,
Klust (1940) described the changes which occur as development proceeds in
several Cyprinid species. Authors who have attempted to correlate the struc-
ture of the alimentary tract with the feeding habits of the fish have already
been reviewed in a previous paper (cf. Al-Hussaini, 1945).
MATERIAL AND METHODS

This work was carried out in the Department of Zoology, Sheffield Univer-
sity, the roach and gudgeon being supplied by the Sheffield Corporation
Water Works from their ponds surrounding the city, while the mirror carp
came from the Surrey Trout Farm (Haslemere). The Red Sea types used for
comparison were collected personally from the neighbourhood of the Marine
Biological Station at Ghardaqa, while other supplementary types came from
various English waters.
The techniques employed are numerous, and it will be more convenient
to refer to them in the appropriate sections of the text with which they are
individually concerned. When an anaesthetic was needed for experimental
work urethane was used, while the fishes were normally killed by a blow on
the head.
In the following account the omnivorous roach is described as the central
type and then compared with the other two species.
THE ANATOMY OF THE ALIMENTARY TRACT

The Protractile Apparatus of the Mouth
The mouth of Rutilus (Text-fig. 1) is small and agrees with the 'normal'
type of mouth described by Gregory (1933) in Micropterus, except that in the
Rutilus both jaws lack teeth. Mouths of this type have a moderate gape and
moderate protrusibility. The maxillae are excluded from the gape and the
premaxillae develop articular and ascending processes.
This latter process, or 'spine', is attached to the ethmoid by the rostral
ligament (R.L.) containing a small cartilaginous nodule. According to Eaton
(1935), this nodule ensures that the ligament shall bend in precisely the
same way each time the jaw Tretracts. The protrusibility of the mouth
depends largely on the length of the ligament which both allows, and
checks, the forward thrusting of the upper jaw, and also on the length of
the premaxillary spine; the larger the spine the more protrusible the mouth
(Eaton, 1943).
The ventral end of the maxilla (MX.) is attached to the premaxilla by a
short flexible ligament near the angle of the mouth. Dorsally the two maxillae
meet and form a groove in which the premaxillary spine and ligament slide
back and forth. The maxillae are also loosely attached to the vomer and pala-
tine, so that when premaxillae are thrust forwards the maxillae do not impede
but rather assist this process, since this dorsal maxillary hinge allows their
ventral ends to thrust forwards with the premaxillae.
ii2 Al-Hussaini—Functional Morphology of the Alimentary
In the lower jaw the dentaries are held together at the symphysis by a very
short ligament allowing a slight amount of movement.
The advantage of a protrusible mouth to Rutilus is that it increases the
range over which the fish can take food as well as enabling it to engulf small
prey or other food particles entire by a quick snap, and thus compensates for
the absence of teeth on both jaws and palate.
R.A. B.D
TZ
DO
.
LAP
TEXT-FIG, I . Lateral view of head of R. rutilus showing protraction of the mouth. The
lacrymal, the posterior part of the operculum with its branchiostegal rays, and part
of the pectoral girdle have been removed, and the anterior part of the body cavity
exposed.
In Gobio the mouth is larger than in Rutilus, and a barb is attached to each
jaw angle. The upper jaw is larger than the lower so that the mouth opening
is directed distinctly downwards. Both the premaxillary spine and the
rostral ligament are longer and hence the mouth is more protrusible than in
Rutilus. When the jaws are fully protruded the mouth opening is completely
ventral, a feature obviously connected with the bottom-feeding habit of
the fish. When roach and gudgeon were kept together the roach would
immediately dash at any food (e.g. insects) thrown in, but the gudgeon
ignored it completely until some had sunk to the bottom of the tank. The
differences in the shape of the mouth and in the length of its constituent
parts represent, therefore, the morphological expression of differences of
feeding habits.
In the herbivorous Cyprinus the head is relatively larger in proportion to
the rest of the body than in either of the other two species. The length of the
rostral ligament and premaxillary spine, and hence the protrusibility of the
mouth, is intermediate between Rutilus and Gobio. There are four barbs,
shorter than those of Gobio, around the mouth, one from each jaw angle and
a dorsal pair from the skin covering the maxillae.
Although Cyprinus feeds more easily from the bottom, yet it can rise to
take food from the surface and hence combines the feeding habits of Rutilus
and Gobio. These differences in feeding habits are also reflected in other
structures. Thus Evans (1940) showed that in Rutilus the eyes and optic
lobes are much larger than in either Gobio or Cyprinus, but in the latter two
species the facial and vagal lobes (concerned with taste) are much better
developed than in Rutilus. Thus Rutilus, with its superior vision, is able to
snap its food freely in the water while Gobio and Cyprinus normally seek it
from the bottom and have developed barbs richly supplied with taste-buds for
this purpose (cf. p. 126).
The Pharyngeal Dental Apparatus

The fifth branchial arch is reduced to a single strong bone on each side,
the 'os pharyngeus inferior' (Goodrich, 1930, p. 440), usually referred to
in cyprinids as the 'pharyngeal jaw'. The modified arch in Rutilus (PI. II,
fig. ya, b, c) is typical of the type described as 'omnivorous' by Chu (1935)
in Chinese cyprinids. Each half of the complete arch is about three times as
long as it is broad, its posterior limb is about one and a half times as long as
the anterior, while at the angle between them there is a distinct lateral
projection just behind the second tooth. The posterior surface is pitted (num-
ber of pits variable) and wing-like. An edentulous process curves strongly
dorsally, making an obtuse posterior angle. This process is compressed and
sometimes tapering. It is directed medially, reaching the otic region of the
skull where it meets its fellow from the opposite side; thus the two processes
form an arch bounding the opening to the oesophagus.
In Gobio (PI. II, fig. 7/) the length of each pharyngeal bone is about four
and a half times the width, the posterior limb is not longer than the anterior
limb, while the pitted surface is narrower than in Rutilus, dimensions which
agree with those given by Chu (1935) for the carnivorous species of the sub-
family Gobioninae in Chinese waters.
In Cyprinus the pharyngeal bones are relatively well developed (PL II,
fig. yd, e). The length of each is only about two and a half times the width
and the two limbs are of about equal length. They are thus massive bones
compared with the other two types.
In all these types, the teeth are affixed to the medio-ventral aspect of each
pharyngeal bone. In Rutilus they are close-set and uniserial, usually five in
each row. Each has a cutting edge. The two posterior teeth (4 and 5) have
recurved tips, forming hook-like processes directed backwards. These teeth,
together with the third, are strongly compressed, but the first two teeth are
stouter and more or less conical with, pointed tips. Sometimes an additional
tooth develops on the left side, a fact already noted by Hubbs and Hubbs
(1944). In their discussion of 'bilateral asymmetry' in vertebrates they quote
the roach (R. rutilus) as an example. Out of 104 specimens examined 79 had
114 Al-Hussaini—Functional Morphology of the Alimentary
asymmetrical teeth, the extra tooth being always on the left, never on
the right. It should be noted that the extra tooth is only found in well-
grown specimens, never in small ones. It therefore appears to be added at
a later age.
The teeth in Gobio are biserial, each bone has a medial row with four or
five teeth and a lateral row with two only. Each tooth is wedge-shaped and
hooked as in the posterior teeth of Rutilus. The medial teeth are stronger
than the lateral and, with the exception of the first which is small, of approxi-
mately equal size. The teeth of the lateral tow lie opposite the third and fourth
teeth of the medial row.
In Cyprinus the teeth are arranged triserially (2:1:1). In the mirror carp
the rows are not quite so sharply defined as in the common carp in which
sub-species there is also an extra tooth (3:1:1). The free ends of the teeth are
rounded, somewhat pointed, but never hooked. All four teeth converge and
collectively form a very strong, stud-like prominence, a feature regarded by
Chu (1935) as of a highly specialized herbivorous type.
Small teeth may he found embedded in the mucous membrane of the
pharynx in the vicinity of the pharyngeal bones. Chu regards these as accessory
growing teeth destined to replace old teeth if these are lost.
A horny pad is developed in the dorsal wall of the pharynx below the
occipital region of the skull opposite to the pharyngeal teeth. In Rutilus this
is more or less ovoid in plan (PI. I, fig. 1, H.P.) and double convex in trans-
verse section (PI. I l l , fig. 8) and fits loosely into a corresponding fossa in a
special masticating process of the basioccipital. Its free surface is rugose and
the pharyngeal teeth bite against it. This pad, together with the alternating
disposition of the teeth, which are thus enabled to shear the food, completes
an exceedingly efficient masticating apparatus.
The pad of Cyprinus is similar to that of Rutilus but even harder, but in
Gobio the pad, trapezoidal in plan, is not nearly so well developed and is much
softer (it can be easily pierced with a needle).
It follows from the above comparison that the entire pharyngeal dental
apparatus is best developed in the herbivorous type (Cyprinus), facilitating the
comminution of plant material, in the carnivorous Gobio the hooked teeth
help to secure and tear the prey, while finally the omnivorous roach is strictly
intermediate with both hooked and shearing teeth.
The gill-rakers are short in Rutilus and Gobio, but are longer in Cyprinus.
Long gill-rakers characterize the majority of bottom-feeders which stir up
the mud—a habit which the carp is known to have (Kyle, 1926). Thus, for
example, they are well developed in the bottom-feeding Mugil auratus and
Upeneus barberinus (Al-Hussaini, 19476) and also in Mulloides, which is a
bottom-feeder and shovels sand, and in Scarus, a coral feeder which grinds
its food into a pasty mass (Al-Hussaini, 1946, 1945). The shortness of the
gill-rakers in Gobio is therefore surprising, especially when one reads in
Regan (1911), describing how Gobio secures its food, that it 'gropes and grubs'
for it.
Tract of Some Fish in Relation to their Feeding Habits. 115
The Mechanism of Deglutition
The jaws are opened to admit food mainly by the action of two pairs of
muscles, namely, the geniohyoidei (Text-fig. 1, GH.), a pair of stout muscles
arising from the first and second branchiostegal rays and ceratohyals and
passing forwards in close apposition to each other to be inserted on the inner
surface of the dentary, and the sternohyoidei (Text-fig. 1, SH.) which arise
somewhat laterally from the cleithra and pass forwards and towards the middle
line to be inserted on the dorsal surface of the urohyal on either side of its
dorsal crest. Thus by drawing the hyoid ventrally and caudally the sterno-
hyoidei augment the action of the geniohyoidei.
The entry of prey or food into the mouth may be still further assisted by
the action of the levator arcus palatini (Text-fig. 1, L.A.P.) which arises from
the otic region of the skull and is inserted into the hyomandibular in Gobio
and Cyprinus and into the hyomandibular and pterygoid in Rutilus. Thus by
raising the hyomandibular (and pterygoid) the mouth cavity is enlarged and
the food sucked into the mouth.
The closing of the mouth after the entry of the food is effected by the
adductor mandibulae, a large, complex muscle lying immediately below
the skin in the cheek region. In Rutilus two portions are distinguishable, the
maxillaris (Text-fig. 1, MX.AD.) and the mandibularis (MD.AD.). The first of
these arises from the preoperculum, passes below the eye, and is inserted by
a strong tendon into the lateral surface of the dorsal portion of the maxilla.
Its contraction lowers the maxilla slightly and thus holds the mouth firmly
closed ag'ainst the pull of the second portion, the mandibularis, on the lower
jaw. The mandibularis portion arises from the hyomandibular, preoperculum,
and quadrate, and runs immediately below the eye to its insertion by means
of a strong tendon on the inner surface of the mandible. In Gobio both
portions are further subdivided, the maxillaris into external and internal
moieties, and the mandibularis into three more or less distinct parts. Cyprinus
is intermediate in that the mandibularis portion is simple like that of Rutilus
while the maxillaris is double and resembles that of Gobio.
In the living fish it may be observed that the roach is able to snap its mouth
closed more quickly than either the gudgeon or the carp, an observation that
may be correlated on the one hand with the single insertion for each portion
of the adductor muscle in Rutilus against the multiple insertions in the other
two species, and on the other with the feeding habits of the fish. Whereas
Rutilus secures food which is moving freely through the water, Gobio and
Cyprinus feed in a more leisurely manner by probing for sedentary food
particles in the mud.
Once the food is securely within the mouth it may be assisted on its
passage to the pharyngeal teeth by the narrowing of the mouth cavity. This
is accomplished by two pairs of muscles. First, the hyohyoideus lies below the
'tongue' in the region of the geniohyoideus. Its action is to raise the 'tongue'
and with it the floor of the mouth. In Gobio and Cyprinus this muscle com-
prises two distinct portions, with a greater extension ventral to the gullet
than in Rutilus. The second muscle constricting the buccal cavity is the
adductor arcus palatini. It lies deep to the levator arms palatini and arises
from the parasphenoid and pro-otic and is inserted into the hyomandibula,
pterygoid, and palatine, thus it draws these elements inwards and forwards.
The area of insertion of this muscle is broader in Gobio and Cyprinus than in
Rutilus.
As the food passes backwards into the pharynx the pharyngeal jaws are
opened to admit it by the action of the pharyngo-clairicularis, a complex muscle
with an 'externus' and an 'internus' portion. Both portions arise from the
anterior surface of the cleithrum and pass in a generally dorso-medial direc-
tion. The 'externus* portion is inserted into the posterior surface of the
anterior limb of the fifth branchial arch while the 'internus' portion is in-
serted partly on the ventral surface of the anterior extremity of the fourth
branchial arch and partly in a similar position on the fifth arch. The action
of this muscle is augmented by that of the trapezius (Text-fig, i, TZ.) a strong
muscle arising from the occipital and otic regions of the cranium and inserted
into the tip of the posterior limb of the pharyngeal jaw. It is best developed
in Cyprinus. The muscle, antagonistic to these two, which draws the teeth
together and on to the surface of the horny pad is the retractor arcus branchialis
dorsalis (Text-fig, i, R.A.B.D.), a very powerful muscle, triangular in outline,
arising from the masticatory process of the basi-occipital just lateral to the
horny pad (cf. PI. I l l , fig. 9), and inserted on the caudal surface of the posterior
limb of the pharyngeal bone. Again it is best developed in Cyprinus, less so
in Rutilus, and much less in Gobio.
Two other muscles are worthy of mention in connexion with feeding,
namely, the constrictor pharyngeus, which passes laterally and somewhat
caudally from the mid-ventral line of the pharyngeal wall, and the inter-
mandibularis (PL I, fig. 2, IM.). This is a very small muscle (some 0-64 mm.
wide in a roach 7 cm. long) passing between the medial surfaces of the dentaries;
it is partially covered by the geniohyoidei. In the Cyprinids, where-only small
food particles are taken, this muscle remains small and only a slight move-
ment is possible between the rami of the lower jaw (cf. also Takahasi, 1925),
but in predatory types of mouth, e.g. Pterois volitans, the two dentaries may
be widely separated during swallowing (Al-Hussaini, 19476) when large prey
is taken. Thus in this fish the intermandibularis is large, as it is in Catostomids
(Takahasi, 1925; Edwards, 1926) and Siluroids (Takahasi, 1925).
Apart from the muscles described above, those operating the operculum
and gill arches during respiratory movements by varying the hydrostatic
pressure within the mouth and pharynx are bound to affect the passage of the
food within.
As already mentioned small pieces of food are normally taken by a quick
snap (less marked in Gobio), but where the prey is larger (e.g. earthworms)
the fish first suck the food with great eagerness and then thrust it out again.
The process is repeated several times till finally the fish, as it evades others,
retires into a corner and indulges in what appears to be mastication. The
respiratory movements are accelerated and in particular the opercula are
swung farther out than in normal respiration. The earthworm may be
recovered from the gullet a short time later torn into pieces.
Thus in summary, the cycle of events occurring just before and during the
capture of prey is as follows. The mandible is depressed and the premaxillae
accordingly thrust forwards by the contraction of the genohyoideus and sterno-
hyoideus, the motion of the mandible being transferred to the premaxillae
by virtue of the ligamentous joint between them (Text-fig. 1, L.) the motion
being limited by the length of the rostral ligament. As soon as the prey is
seized and contained in the buccal cavity the two adductor mandibulae are
simultaneously contracted, thus closing the mouth, the mouth cavity is
narrowed by the contraction of the adductor arcus palatini and by the
elevation of the mouth floor, thus pushing the food back towards the pharynx.
The mouth is then opened again and the buccal cavity and the pharynx are
dilated (the latter by the various muscles attached to the gill arches), and
water is sucked in through the mouth. The prey is thus washed still farther
backwards. In the next movement, that of closing the mouth, the pharyngeal
floor is raised by the contraction of the constrictor pharyngeus, thus forcing
the prey into the region of the teeth. Here, through the action of the retractor
arcus branchialis dorsalis, trapezius, and pharyngo-clavicularis, the teeth can
work alternately against each other, squeezing the prey between the two
'jaws' and against the horny pad, and finally pushing it backwards into the
oesophagus. This 'masticating' action seems to be the more laborious part
of the feeding process as observed in the living animal. It should be noted
that a Cyprinid fish can hold its food and break it down by its teeth con-
currently with the respiratory movements; in other words, deglutition and
respiration do not interfere with each other. This is made possible by the
position of the 'pharyngeal jaws' at the entrance to the gullet, that is posterior
to the gills.
The Intestinal Tube

In all three examples the oesophagus, more or less cylindrical in form,
occupies an oblique position in a cranio-caudal direction (Text-fig. 1; PI. I,
fig. i, ES.), owing to the postero-ventral growth of the masticating process of
the basi-occipital. It is remarkably short (4 mm. in a roach 175 mm. in length)
and is delineated from the intestine by a constriction. The pneumatic duct
(Text-fig. 1, P.D.), carrying a small dilatation at its extremity, opens into the
dorsal aspect of the oesophagus.
The alimentary canal posterior to the oesophagus increases suddenly in
diameter forming an intestinal swelling (Text-fig. 1, i.s.) as in all other
Cyprinids so far described by various authors and in Atherina (Al-Hussaini,
1947a) and several labroid fishes (Al-Hussaini, 19476). The swelling is a
straight tube, gradually decreasing in diameter as it extends caudally, close to
the dorsal body-wall, nearly as far as the posterior end of the air-bladder,
from which point it curves sharply forwards again making one siphonal loop.
n8 Al-Hussaini—Functional Morphology of the Alimentary
In Rutilus the distal limb of this loop, which reaches as far forwards as the
transverse septum, is of smaller but constant diameter. It turns caudally once
more and, coursing on the left of the siphonal loop, terminates at the anus.
Sometimes the bend where the second and third limbs join one another has
an upward tilt (Text-fig. 2A). The last portion of the third limb is tapering
and corresponds to the rectum. Now it is true that in the cyprinids there is
no ileorectal valve separating the intestine from the rectum as in most
• 2 3 limb
TEXT-FIG, Z. The intestine as it appears in situ from the left side; A, R. rutilus; B, G.
gobio; E, Cyprinus carpio; F, the intestine of Cyprinus carpio from the ventral aspect,
c, D, and G diagrammatic representations of figs. A, B, and E respectively.
teleosts, but the fact that the last, tapering portion of the intestine has
different histological features (cf. p. 134) is considered sufficient justification
for designating .it rectum. For a contrary view, reference should be made to
Jacobshagen (1937), who considers that cyprinids, mormyrids, and some
others do not have the mid-gut differentiated from the hind-gut.
In Gobio (Text-fig. 2B, D) the distal limb of the siphonal loop is short, the
intestinal swelling extending only as far as the middle of the anterior lobe of
the air-bladder before turning back. In Cyprinus (Text-fig. 2E, F, G) the
intestine is longer and its looping more complex. The intestinal swelling, or
first limb of the intestine, extends^caudally throughout the whole length of the
body-cavity, the intestine then curves sinistrally upwards and forwards to
the middle of the body-cavity, and then backwards again in a sigmoid manner,
becoming dextral once more as it approaches the posterior extremity of the
body cavity. Here it doubles forwards again and courses anteriorly to the
septum transversum, taking an upward and sinistral course, then back once
more with a hairpin loop, then forwards to the middle of the body-cavity
and finally, with another sharp loop, it turns caudally and ultimately opens
to the exterior at the anus. In the morphological sense the intestine of
Cyprinus may still be regarded as formed of one and a half siphonal loops, as
in the other two species, but the second and third limbs are strongly curved
in the middle and shifted to the right (Text-fig. 2, compare G with c). This
description was made from specimens of about 12 cm. in length, but according
to Smallwood and Smallwood (1931) the intestine becomes much more coiled
in large specimens of the common carp. It should be noted that the coils of
the second and third limbs lie to the left of the first limb in all cases and that
the proximal limb bears the swelling and is nearly straight in all three species,
while the second and third limbs are shortest in the carnivorous Gobio and
longest in the herbivorous Cyprinus.
The liver (hepatopancreas) grows round most of the intestine. The gall-
bladder lies between the anterior lobe of the swim-bladder and the intestinal
swelling, and its duct opens into the right side of the latter very slightly
posterior to the oesophagus. The pancreatic duct accompanies the bile-duct,
but it is difficult to find in gross anatomy.
Fatty tissue fills up the spaces between the three limbs of the intestine
along its entire length and contains microscopic pancreatic alveoli embedded
within it.
The blood-supply to the intestine is derived from a coeliaco-mesenteric
artery which leaves the aorta just posterior to the pharyngeal dental apparatus.
The Mucosal Folds
In all three forms the mucous membrane along the inner edge of the upper
jaw is produced into a crescent-shaped maxillary valve (PI. I, fig. 1, MX.W),
papillated on its ventral surface. Contrary to the majority of teleosts an
opposing mandibular valve is wanting, and thus the maxillary valve must
operate against the floor of the mouth.
On the roof of the mouth there are several longitudinal folds which may
be branched, or even swollen, and in the region opposite the 'tongue'
they are papillated. In Gobio there are two distinct protuberances a little
posterior to the maxillary valve. These will be referred to as 'palatine
cushions'.
In all three species the pharynx is differentiated into two distinct regions,
an anterior (PI. I, fig. 1, A.PH.) and a posterior (P.PH.) proportioned to each
other as 2:1. Functionally, the anterior pharynx containing the gill-slits is
concerned with respiration, while the posterior pharynx containing the horny
pad and pharyngeal teeth has an alimentary purpose. The mucosal folds
increase in complexity as they run backwards (cf. PL I, fig. 1).
In Cyprinus the roof of the anterior pharynx is very 'fleshy' and exhibits
an interesting response to mechanical stimulus—found to a less extent in the
other two species. When pierced with a needle it swells considerably and then
i2o Al-Hussaini—Functional Morphology of the Alimentary
gradually subsides. The reaction is shown even by a recently killed specimen
from which histological samples were being taken.
The mucosal folds lining the intestine vary somewhat from one region to
another. Various observations have been made concerning their pattern in
sundry fishes by earlier workers, notably by Eggeling (1907) and Klust (1940).
In Rutilus there are some 10-12 longitudinal folds in the oesophagus which
are continuous with the folds of the intestinal swelling. In the intestinal
swelling the folds run in various directions, branch, and reunite. They are
relatively broad, being about 0-33 mm. across when seen in surface view
(PI. I, fig. 1). The folds are particularly dense and crowded in the first centi-
metre of the swelling but become less so farther back. By the time the proximal
part of the third limb of the intestine is reached, the mucosal folds are pre-
dominantly transverse in direction although they may still decussate. The
distal five-sixths of the third limb exhibits a transverse zigzag pattern in the
mucosal folds reminiscent of the arrangement of myomeres in the dogfish.
The folds are also much thinner when seen in section (about four folds to the
millimetre) and the mucosa has a brownish colour which is highly characteris-
tic of this part of the intestine. About a centimetre before the anus is reached
a faint line may be seen from the mucosal surface passing transversely round
the intestine at the place where, in most fishes, the ileorectal valve occurs.
The mucosal folds of the part of the intestine between this line and the anus
(i.e. the rectum) assume a longitudinal direction, show only a few inter-
connexions, and become thicker once more.
In Gobio the mucosal folds resemble those of Rntilus except that those of
the third limb of the intestine assume a longitudinal rather than zigzag orienta-
tion, and in the rectum the interconnexions between them become more
numerous. In Cyprinus the folds of the third intestinal limb resemble those
of Gobio but the condition in the rectum is more like Rutilus.
The four segments of the intestine can therefore be conveniently recognized
by the following characteristics: the intestinal swelling, or first limb, has a
greater diameter and the mucosal folds are complex, the second limb has a
smaller and uniform diameter and less complex mucosal folds, while the third
limb, similar in diameter to the second limb, is characterized by its brownish
colour and narrow mucosal folds, and finally the rectum is tapering and its
mucosal folds are longitudinal.
The Surface Area of the Intestinal Mucosa

The surface area of the intestinal mucosa is of great importance since it is
this area which is concerned with the absorption of food. Warren (1939)
adopted an excellent technique for measuring this in the dog which was
modified by Wood (1944) and applied to cats and rats. The basic principle
of the method is to inflate the intestine to a known and constant pressure
(60 cm. of water for the dog) with saline and then fix it in this condition and
finally cut micro-sections of it in transverse and longitudinal planes. These
can be projected at a known magnification on to paper and the linear dimen-
sions of the serosal surface and of the mucosal surface in both directions can
be measured by a rotometer. If now sc = serosal circumference, SL —
serosal length, SA = serosal area, MC = mucosal circumference, ML = mucosal
, 1 , /MC ML\ MA r
length, MA = mucosal area, then in general I— X —I > — for an irregular
surface. However, as Warren shows, a serviceable approximation for the
mucosal area (MA) can be obtained by the following formula, where EA = the
, EA MC ML . ..
estimated mucosal area. — = 1. ML, MC, SC, and SL are all
SA SC SL
measurable quantities, while SA is easy to calculate if the length of intestine
under review is assumed to be a cylinder. This last assumption is not quite true
for the fish gut since at one end the intestinal swelling and at the other the rectum
are of inconstant diameter, and further, since it has been shown that the
entire gut is absorptive {vide infra) the mere introduction and ligation of
cannulae into the ends will produce an unavoidable error into the measure-
ments of serosal and mucosal length. Nevertheless these errors are more or
less constant for all three types examined and the data have therefore at least
a comparable significance between them. Using Wood's modification, the
precise procedure was as follows. The intestine was cut into two parts, viz.
the first limb (swelling) in one part and the remainder of the intestine in the
other. One end of each piece was attached to an end of the horizontal limb
of a _L-shaped glass tube, the vertical limb of which was of such a length as
to give the desired hydrostatic pressure to distend the intestine. The free ends
of the two pieces of gut were then joined to the two limbs of a A-shaped glass
tube, the upright limb of which was connected to a wash-bottle to which a
sphygmomanometer bulb was attached. On gently raising the pressure in the
wash-bottle by means of the bulb the fluid contents of the bottle could be
driven at a steady and constant pressure through the two portions of intestine
simultaneously and up the vertical glass tube till it trickled out of the open
end of this tube. The contents were first washed from the gut in this manner
using the isotonic solution recommended by Young (1932) for fresh-water
fishes followed by 10 per cent, formalin as a fixative. The data thus obtained
are given below in Table 1.
Several interesting relationships-may be deduced from this table. First
the relative length of the gut (R.L.G., column 3) is nearly constant for each
individual species, a feature already noted in other fish, but in Rutiltis it is
smaller than is usual for omnivorous species (i*3~4'3) while Cyprinus also
has a smaller R.L.G. than the normal range for herbivorous fish (3-7-60);
Gobio, on the other hand, lies within the normal range for carnivores (0-5-2-4)
(Al-Hussaini, 19476). The small R.L.G. of Rutilus and Cyprinus together with
the simplicity of the gut (absence of stomach and pyloric caeca) may be
peculiar to these species, but a considerably more extensive survey would be
needed to settle this point.
The ratio between the estimated mucosal area and the serosal length
(columns 6 and 9) is greater for the intestinal swelling than for the rest of the
TABLE I . Measurements of the Absolute Length of the Intestine, Mucosal Area, &c, in Rutilus rutilus (Ri-6), Gobio gobio
(G7-12), and Cyprinus carpio (C13-15)
1 2 6 8 IO n 12
fe
3 4 5 7 9
Length Estimated
s
Length Length of 2nd mucosal
offish Total SL/FL = of 1st Estimated and 3rd area of 2nd EA! + EA2 =
less length R.L.G. limb 0/ mucosal limbs of and 3rd Total estimated
caudal of in- (rela- intestine area of intestine limbs of in- mucosal area Weight EA/WF =
Fish fin in testine tive in first limb in testine in of intestine offish mucosal
no. mm. in mm. length mm. in cm.z mm. cm.2 in cm.z in gm. coefficient
= FL = SL ofgut) = SL! = EAt EA^SLj = SL 2 = EA2 EA 2 /SL 2 = EA = WF = QM
Ri 95 IOO 1-05 2O 836 4-18 80 23-85 3-i8 32-21 14-0 239
R.2 142 155 1-09 35 25-27 722 120 6048 5-°4 85 65 56-0 i-57
R3 155 165 1-06 45 42-08 935 120 74-16 618 n6'»4 75-5 i-53
R4 158 140 0-90 35 27-48 7-85 IO5 71-19 6-78 9867 660 1-50
R5 185 183 1-oo 48 5491 11-44 135 102-51 763 157-42 104-0 i-5i
R6 185 185 i-oo 46 51-38 1117 139 11485 827 166-23 IO5-5 1-58
G7 101 69 o-68 21 11-13 5-3© 48 I5-55 324 2668 II-O 2-42
G8 103 74 0-72 25 13-75 550 49 1798 367 3178 131 241
G9 104 75 0-72 25 1573 629 SO 1875 3-75 34-48 160 2-15
Gio 116 88 0-76 3° 22-53 7-51 58 1844 318 4097 192 213
Gn 119 IOI 085 32 21-54 6-73 69 2546 369 47>oo 22-0 2-14
G12 232 ft:
120 102 0-85 32 20-54 6-42 7° 28-91 413 49-45 2-13
C13 75 140 1-87 20 766 3-83 120 21-48 1-79 2914 II-5 2-53
C14 76 140 1-84 2O 962 4-81 120 2496 208 34-58 135 2-56
C15 98 180 1-84 3O 1692 5-64 150 3300 2-2O 4992 2O2 2-50
intestine, a feature obviously to be correlated with the complexity of the
mucosal folds. Further, although the estimated mucosal area is absolutely
greater in the larger compared with the smaller fish (cf. columns i, 10, and 11)
because the mucosal foldings grow with the fish, nevertheless it is relatively
smaller (cf. Ri with R5 and R6). In this connexion it must be remembered
that the animal in its growing stage needs a relatively greater quantity of food
and hence has a greater absorptive area per unit of body-weight. This ratio
between the mucosal (absorptive) area and the body-weight (mass of tissue
requiring food), which I have called the mucosal coefficient, is expressed
numerically in column 12. So far as mammals are concerned Wood (1944),
working on cats and dogs of practically equal weight, found by measurement
that the ratio is constant in both mammals, while Cori (1925), using growing
rats of varying weight, deduced a constant ratio from the quantities of sugar
absorbed.
Referring again to the Cyprinid fish, it may be seen that in Gobio the mucosal
coefficient becomes nearly constant by the time the fish has attained a length
of n o mm. and a weight of about 15 gm. Again, if the mucosal coefficients
of the three fish are to be compared and related to their varied diets it should
be done with fish of approximately the same weight. This has been done in
Table 2.
TABLE 2. Relative Length of Gut and Mucosal Coefficient of Three Species of
Fish of approximately Equal Weights
Estimated
Intestinal mucosal
length Body- area in
No. in in mm.. weight cm.2 Mucosal
Species Table I = SL in gm. = EA coefficient R.L.C
Gobio gobio G8 74 131 31-78 2-41 0-72
Rutilus rutilus Ri 100 14-0 33-52 239 105
Cyprinus carpio .. C14 140 135 34-58 256 1 84
An examination of the table shows that Cyprinus has the highest R.L.G.
and Gobio the lowest, and although the mucosal area follows the same
sequence the difference is very much less marked. Thus one is led to the
important deduction that the shortness of the intestine may be compensated
by an increase in the complexity of the mucosal foldings. It should, never-
theless, be borne in mind that the longer intestine, although having a mucosal
coefficient very little greater than the short one, probably has the advantage
of retaining the food for a longer period and may still be regarded as an
adaptation to herbivorous diet provided that the comparison is made between
closely related species living under fairly similar conditions.
THE HISTOLOGY OF THE ALIMENTARY TRACT

For this study serial sections were made from specimens measuring 65-
100 mm. long. The material was fixed and decalcified simultaneously in
Boling's modification of Bouin's picro-formol (Cowdry, 1943, p. 188) and
stained in Delafield's haematoxylin-eosin, certain details being subsequently
verified by using Mallory's triple connective-tissue stain, Mayer's muci-
carmine, or Giemsa's method for paraffin sections. Individual cell types were
studied by the maceration method of Goodrich (1942). In addition to these
methods the oesophagus and intestine were removed from specimens of
different sizes and fixed in Bouin, Maximow, or Susa and stained with
Heidenhain's iron-alum haematoxylin-eosin.
The Buccal Cavity

The buccal cavity of Rutilus is lined by a stratified epithelium containing
taste-buds and mucus-secreting cells and resting on a basement membrane
supported by a stratum compactum (PI. I, fig. 2). The sub-epithelial con-
nective tissue is differentiated into a tunica propria in juxtaposition to the
epithelium and a deeper, looser tissue known simply as the submucosa, a
condition similar to that found in all fishes studied earlier (Al-Hussaini,
1945-7)-
At the entrance to the mouth cavity the epithelium is thick and the outer-
most layers are formed of strongly cornified polyhedral cells. In these
respects it resembles the epithelium of the outer skin but differs from it in
that both mucus-secreting cells and taste-buds are absent; both of these struc-
tures occur in the skin. Further, the 'Kolbenzellen', characteristic of the
skin of certain teleost families (Uhlich, 1937), are absent. Such cells have
been described from the buccal epithelium of Calamoichthys (Purser, 1926).
They have a central nucleus embedded in a clear cytoplasmic fluid which
does not show the staining reactions characteristic of mucus.
A very short distance within the mouth opening taste-buds begin to appear
in the sections and rapidly become numerous as one passes backwards; they
are particularly numerous on the ventral surface of the maxillary valve.
According to Herrick's (1903-4) view of the direct correlation between the
density of taste-buds and the delicacy of the sense of taste in fishes, Rutilus
should have a well-developed sense of taste in both the skin and the mouth.
In Rutilus each taste-bud is a flask-shaped structure measuring about 100/i.
by 20 [A and in general structure similar to those already described in Mulloides
(Al-Hussaini, 1946).
By the time the middle of the maxillary valve is reached taste-buds have
become the predominant feature of the buccal epithelium and are found all
over the mouth cavity except on the dorsal surface of the maxillary valve. On
the other hand, mucus-secreting cells, which have already made their
appearance at this level, are plentiful just where taste-buds are absent or
sparse, namely, on the dorsal surface of the maxillary valve and the roof of the
mouth. Towards the posterior end of the valve taste-buds and mucus-
secreting cells are nearly equally distributed on both the roof and floor of the
mouth. At the sides of the mouth, which in transverse sections appear as two
recesses, both elements are scarce.
The mucus-secreting cells are mostly of the pyriform type (cf. Al-Hussaini,
1945, p. 368, for terminology of mucus-secreting cells) and are concentrated
along the crypts of the buccal epithelium rather than on the folds. Although
assuming no particular pattern they become more numerous as one passes
caudally towards the pharynx while the taste-buds show a reverse tendency
(Text-fig. 4).
A possible explanation of this differential distribution is that the mucus
secreted by numerous cells on the opposing surfaces of the dorsal aspect of
as M Ess
m
1 I / H^i
TEXT-FIG. 3. Constituent cells of the stratified epithelium of the bucco-pharynx of

R. rutilus obtained by Goodrich's maceration method: (<z) from the stratum germina-
tivum; (ft) from the second layer; (c, d) from intermediate layers; (e) from the
superficial layer; (/) a pyriform and (g, h) saccular mucus-secreting cells.
the maxillary valve and the roof of the mouth prevents their adherence and
facilitates the movement of the valve during respiration. They are otherwise
absent from the extreme anterior part of the mouth since lubrication of the
food is not necessary until after the food is in the mouth, and swallowing has
commenced. The taste-buds, on the other hand, are concentrated very early
so that the food may be immediately sampled.
The mouth floor, or 'tongue' region, shows no special histological features
which differentiate it from other areas of the mouth.
The cells in the basal layer (Text-fig. 3a) are formative and from them the
other cell types are derived. The cells of the intermediate layers are frequently
polyhedral and have their angles drawn out into short processes which, by
interlocking with similar processes from neighbouring cells, presumably give
a firmer and tougher structure to the entire epithelium. Within the layer of
cells immediately adjoining the basal layer certain spheroidal cells may be
found, each with a short process housing the nucleus. Similar cells may be
found in the succeeding layers as the surface is approached, but they tend to
get larger and the nucleus becomes compressed at the base rather than con-
tained in a process (/, g, h). It would thus appear that the pro-mucus-secreting
cells are differentiated along with the stratified cells from the basal layer, and
that mucus secretion is commenced very early in the course of their differentia-
tion, the amount of secretion being gradually increased as the cells approach
the surface.
The basement membrane, stratum compactum, tunica propria, and sub-
mucosa are similar in general structure to those described in the earlier papers.
In the floor of the mouth, in the region of the 'tongue', the submucosa con-
tains large adipose cells which persist back to the heart region.
In both Gobio and Cyprinus the barbs on the lips are very richly supplied
with taste-buds, but, in addition to these, taste-buds are much more abundant
both on the lips (PL I, fig. 3) and in the buccal epithelium than in the
roach.
The order of the three fish on the basis of the abundance of taste-buds is
Cyprinus, Gobio, Rutilus. It is surprising to read in Curry's account (1939)
that taste-buds are not numerous in the floor of the mouth of the common
carp and that they 'are more numerous on the flap than in any part of the buccal
cavity'. By'flap'she presumably means the maxillary valve. In contrast to'
this the mirror carp possesses very numerous taste-buds over the entire
lining of the buccal cavity except on the dorsal surface of the maxillary valve
(PL I, fig. 2). In fact I have not yet examined a fish with more abundant
taste-buds than the mirror carp, and, further, they are of larger size than those
of either Gobio or Rutilus.
In Gobio the two convex 'palatine cushions' before mentioned (p. 119) are
richly supplied with taste-buds and pyriform mucus-secreting cells, the latter
being specially concentrated along the sides of the crypt which separates the
two cushions. The sub-epithelial connective tissue is richly vascular, and
contains numerous collagen fibres and nerves. An attempt was made to
demonstrate the action of these cushions experimentally by first anaesthetizing
a fish and then presenting it first with a piece of gravel, and then with food
(meat) of similar size held close to the mouth. Every time without exception
the particles would be sucked in with the respiratory current and on touching
the cushions the gravel would be immediately rejected, but the food particles
would be retained, at least for some time. It is thus clear that the cushions
act as food selectors and, at the same time, act as an efficient barrier to the
passage of all other material entering the mouth, allowing it to be immediately
rejected. The significance of such a mechanism is self-evident when one
recalls the bottom-feeding, mud-grubbing habits of the fish. The highly
specialized gustatory sense of both Cyprinus and Gobio, in which they also
resemble Mulloides auriflamma (Al-Hussaini, 1946), is clearly an adaptation
to the bottom-feeding habit.
The Pharynx
The Anterior Pharynx
In all three fish the mouth merges gradually, with no abrupt change, into
the pharynx. The mucus-secreting cells become gradually more numerous
and tend to become concentrated along the sides of the crypts so that, in
10 mm.
TEXT-FIC. 4. Diagrammatic representation of the distribution of taste-buds and
mucus-secreting cells in the fore-gut of R. rutilus. A, the roof; B, the floor of the
mouth, pharynx, and oesophagus. Taste-buds open circles (o), mucus-secreting cells
solid (•).
transverse section, they have the appearance of multicellular glands (PI. II,
fig. 5). In some places they become huddled together and stratified, and en-
croach upon theundifferentiated epithelial cells which, although multi-layered
high up on the sides and on the crests of the folds where mucus-secreting cells
are few, are reduced to a single layer at the bases of the crypts. This arrange-
ment resembles that found in other fishes I have previously investigated and
described.
Taste-buds remain numerous, especially in Gobio and Cyprinus; in the
lateral portions of the anterior pharynx of the latter fish especially they form
an almost unbroken sequence (PI. I, fig. 4), while on its roof there is the
palatal organ of Valatour, with its acknowledged gustatory function (Herrick,
1904).
The foregoing account concerning taste-buds and mucus-secreting cells
conforms closely to the generalization which I drew concerning the pharynx
in teleosts (Al-Hussaini, 1946), namely, that it is a region concerned with
gustation as well as mucus production, irrespective of the kind of diet of the
fish, and that the relative extent of these two functions is slightly altered when
the food contains a great amount of silt, as, for example, in Scarus and Mul-
loides. An additional feature is a high concentration of both taste-buds and
mucus-secreting cells on the gill-rakers in the Cyprinids (PL II, fig. 6).
Presumably the mucus serves to trap fbod particles detected by the taste-
buds and so prevent their ejection with the respiratory current, but an
attempt to demonstrate this experimentally led to indefinite results since
direct observation of this region of the pharynx could only be made at the
expense of normal respiratory movement.
Concerning the sub-epithelial structures of the anterior pharynx in general
the following noteworthy points may be mentioned. The stratum compactum
is thinner than in the mouth, in fact in some places it is difficult to detect.
In the tunica propria there are numerous striated muscle fibres (PL I, fig. 4).
In general these are arranged singly and transversely but they may run in
various directions and may be assembled in groups. A striking feature of these
muscle-fibres is that in several places they are closely associated with the
stratum compactum, while they also invade the cores which support the taste-
buds. They presumably serve to mobilize these structures as well as the
general mucosa of the pharynx during the processes of mastication and
swallowing. The large adipose cells already noted in the submucosa of the
floor of the mouth extend also into the pharynx and are found in addition
in the roof but not at the sides of this cavity.
The submucosa of the pharyngeal roof is much thicker in Cyprinus than
in either Gobio or Rutilus, thus accounting for its more 'fleshy' appearance,
while its nerve-supply is very rich—a feature obviously to be correlated with
the profusion of taste-buds found in this species.
The Posterior Pharynx
The mucosal folds of this region are high; they branch and anastomose
freely. Mucus-secreting cells abound (Text-fig. 5c) and attain their maximal
development in this region, being of the saccular type (Text-fig. 3^, h).
Taste-buds are still numerous, although in Rutilus, but not in Gobio or
Cyprinus, they become much less abundant posteriorly.
The horny pad, characteristic of the roof of the posterior pharynx, consists
of an especially thick stratified epithelium (PL III, fig. 8). Of the three easily
recognizable zones the basal (B.Z.) consists of a single layer of cells following
the sinuosities of the tunica propria underlying it. The middle zone (M.Z.)
comprises large polygonal cells, the cytoplasm of which stains deep red with
eosin and crimson with Mallory's triple stain, while the nuclei remain pale
and show nucleoli. The cell membranes are much thickened, and fine
cytoplasmic bridges connecting neighbouring cells together are clearly visible.
The number of layers of cells forming the superficial zone (s.z.) is about equal
to those of the middle zone in Rutilus but is smaller in Gobio and larger in
Cyprinus. Although the individual cells of the superficial zone also have
thick membranes they show a highly characteristic and very irregular outline
as if crumpled and distorted. They take a bright-red colour with eosin and
stain orange with Mallory: thus the superficial zone is sharply contrasted to
the one below it. The nuclei are retained but in a very degenerate condition,
although Curry (1939) described and figured similar cells in the common carp
as 'enucleated'. The superficial cells are shed from the surface either singly
or in groups. The superficial zone does not occur on the anterior or posterior
extremities of the pad, which exhibits here a somewhat attenuated form.
The staining reactions of this zone are those characteristic of horn, and the
hardness of the pad is in direct proportion to its thickness, being greatest in
the herbivorous and least in the carnivorous example.
Numerous coarsely striated muscle-fibres are found at the base of the pad,
which presumably would be capable of effecting some adjustment of its
position. The stratum compactum is very thin in the posterior pharynx and
is composed of only a few compact collagen fibres.
The histology of pharyngeal teeth has already been described in Mulloides
(Al-Hussaini, 1946) and the present fishes exhibit similar features except
that their teeth are firmly fixed to the underlying pharyngeal bones.
The Oesophagus
The oesophagus is customarily defined in higher vertebrates as the transi-
tional region between the pharynx where the glottis opens and the stomach,
so on this basis it must be regarded in the Cyprinids as the region of the gut
extending from the horny pad and pharyngeal teeth to the point where the
intestinal epithelium begins, or rather to the constriction (pyloric sphincter)
at the commencement of the intestine (PL III, fig. 9). Only the ventral and
lateral aspects of the oesophagus are covered by serosa, immediately beneath
which is a dense layer of striated muscle. This single muscle layer, although
of a general circular character, is not precisely transverse to the longitudinal
axis of the oesophagus which is itself oblique. At the junction between
oesophagus and intestine the oesophagus undergoes a pronounced thickening
and forms a pyloric sphincter (M.C). A pyloric sphincter has been recorded
in the goldfish by McVay and Kaan (1940), but no reference was made to it
by either Rogick (1931) in the minnow or Curry (1939) in the common carp.
The submucous connective tissue is very compact and contains many coarsely
striated muscle-fibres which run haphazardly in various directions and which
extend up the very base of the mucosal epithelium, being separated from it
only by a very thin stratum compactum consisting of a very few collagen fibres.
The mucosal folds of the anterior end of the oesophagus resemble, in
general, those of the posterior pharynx; their branching system, giving rise to
primary and secondary folds, has already been described for the common carp
by Edinger (1877) and Oppel (1896). Taste-buds are still plentiful in Gobio
and Cyprinus but are very scarce in Rutilus, while mucus-secreting cells of the
saccular type are present in all three. At the caudal end of the oesophagus
the mucosal folds become very much deeper and the stratified squamous
epithelium characteristic of the crypts and bases of the folds changes to a
h c
1 • 1
/ 0 100M i
TEXT-FIG. 5. Schematized drawings of individual mucosal folds from various parts of

the alimentary canal of R. rutilus. Only the goblet cells, among the various types of
mucus-secreting cells, are shown in black, (a) buccal cavity; (6) anterior pharynx;
(c) posterior pharynx, lateral wall; (d) oesophagus; (e) intestinal swelling; (/) second
limb of intestine; (g) third limb of intestine; (h) rectum.
columnar epithelium as the crest of the fold is approached (Text-fig. 5^).

This columnar epithelium contains mucus-secreting cells of the goblet type
only and no taste-buds.
The arrangement just described is the reverse of that found in the common
carp by Curry (1939), while in the minnow Rogick (1931) described a mixture
of epithelial types in the mucosal folds of the oesophagus.
From the foregoing study and from knowledge gained from three fish
studied earlier (Scarus, Mulloides, and Atherina, Al-Hussaini, 1945, 1946,
1947a) it is possible to reach two important conclusions concerning the
morphology of the oesophagus in teleosts. Firstly, the mucosa changes
gradually from a stratified epithelium with saccular mucus-secreting cells to
a columnar epithelium with mucus-secreting cells of the goblet type. Secondly,
its muscular coat consists of a dense layer of striated fibres circular in direc-
tion. In Atherina alone a layer of longitudinal fibres occurs internal to the
circular layer, and in all the examples studied the submucosa, and even the
tunica propria, always contains scattered muscle-fibres. The pyloric sphincter
is formed by the thickening of the circular layer.
Thus the oesophagus is distinguished from the pharynx on the one hand
by its first mixed and then purely columnar epithelium, and from the intestine
on the other by the type and arrangement of its musculature (in fishes with a
stomach the multicellular 'cardiac' glands may serve as a posterior diagnostic
boundary). It is hoped that this account may help in clearing away the vague
definitions so much in vogue. As thus defined the oesophagus of the Cyprinids
here studied shows no adaptation to feeding habits apart from the fact that
taste-buds are more extensive in the anterior region in Gobio and Cyprinus
than in Rutilus,
Immediately posterior to the horny pad the pneumatic duct opens into
a short dorsal diverticulum formed by two major folds of the oesophagus, at
which point the mucosal cells of the oesophageal folds become columnar.
The duct, near the opening, is ensheathed by a thick layer of fibrous tissue;
to the outside of this is a dense layer of longitudinal striated muscle-fibres
which is in turn surrounded by a similar layer of circular fibres. Presumably
these fibres regulate the opening and closing of the aperture of the duct.
The Intestine
The intestine is lined by a simple columnar epithelium comprising only
two principal types of cells but containing also two or three other subsidiary
cell-types which will be dealt with in detail below. The more common of the
two principal types is that usually described, even by recent authors (e.g.
Maximow and Bloom, 1945, and Clark, 1945), as 'columnar' or 'cylindrical'
on account of their appearance in normal micro-sections. As will be shown
later, the shape thus seen refers to a part of the cell only; the other part, not
easily seen in sections, is variable according to the position of the cell in the
mucosal fold. Following the lead recently given by Baker (1944) the term
'absorptive cells' is used in the present paper, thus putting emphasis on their
function rather than their shape.
The true shape of these cells is revealed by the maceration method of
Goodrich (1942). It will be seen (Text-fig. 6) that the majority are not straight
but, in addition to a general tapering towards the base, each cell is bent at
least once. These bends do not all occur at the same level but interlock with
similar bends in neighbouring cells and this, presumably, serves to strengthen
the epithelium as a whole. The nuclei are variously disposed within the basal
portions of the cells; their presence always involves a bulging of the cell
132 Al-Hnssaini—Functional Morphology of the Alimentary
outlines, which by interdigitating with the swollen nuclear portions of neigh-
bouring cells further serves to strengthen the epithelial sheet. The basal
terminations of the epithelial cells, which may be knob-like (c,f) or finger-like
(a, d), serve to anchor the cells to the subjacent tissues. Sometimes several
cells may be anchored together by this means (e). The free border, at least in
the intact epithelium, seems to be continuous from one cell to another.
TEXT-FIG. 6. Drawings of isolated cells from the intestinal epithelium of R. rutilus. (a),
(c), (d), and (c), absorptive cells; (6) goblet cell; (/) absorptive and goblet cells in
apposition.
Only two previous attempts to study the intestinal cells of fishes by a macera-
tion method appear to have been made. The first, by Edinger (1877), working
with the common carp, reveals simply an inverted conical structure ending in
a filamentous process, and shows neither the perinuclear swelling nor the
-terminal nodules or processes. The second attempt was by Stirling (1884),
using the herring as material. His figures of the cells between the oesophagus
and the cardia of the stomach resemble Edinger's except that the filamentous
basal process is shorter.
Macklin and Macklin (1932) put forward the idea that the spaces between
the filamentous processes of the absorptive cells are not separate inter-
cellular spaces but one continuous space, filled with fluid which freely com-
municates with the tissue fluid in the cavities of the sub-epithelial core,
either by diffusion through the permeable basement membrane or possibly
by actual minute perforations. Thus what may be termed the 'excretory
area!, or the surface area across which substances may diffuse from the
absorptive cells to the body fluids, is enormously increased by this tapering
of the basal portions of the epithelial cells. In Gobio the cells are shorter than
in Rutilus and Cyprinus and hence the 'excretory area' is accordingly smaller.
The second of the two principal cell-types found in the intestinal epithelium
is the mucus-secreting cell. These are typical goblet cells (Text-fig. 66, / )
which attain their maximum concentration in the rectal epithelium (Text-fig.
$e-h)—a fact which, surprisingly enough, has hitherto escaped the attention
of investigators. This high concentration of goblet cells in the rectal mucosa
obviously facilitates defaecation.
Other cellular structures which may be observed within the intestinal
epithelium include small lymphocytes which, although commonest within
the fluid-filled intercellular space around the bases of the absorptive cells,
may migrate between them to within a short distance of the free border. A
second type consists of granular cells (absent from Gobio). These are parti-
cularly abundant in the submucosa and, although they may invade the basal
part of the epithelial layer, they do not migrate so near to the free border as
do the lymphocytes. (This is in marked contrast to the condition observed
in the three fish studied earlier, Al-Hussaini, 1945, 1946, 1947a.) They may
also be found in the connective tissue between the two muscle layers and
beneath the serosa and will be discussed in more detail in Part II of this paper.
Finally, a third type of cell, of infrequent occurrence, comprises cells, pear-
shaped in outline, which reach the free border and are recognizable by their
cytoplasmic inclusions and spheroidal nucleus. Their precise significance is
obscure and they will be dealt with in more detail in a subsequent paper.
Regarding the sub-epithelial tissues, the stratum compactum, better
developed in Gobio than in Rutilus or Cyprinus, lies in close proximity to the
epithelium and not in the middle of the submucosa as in the Salmonidae
(Oppel, 1896; Greene, 1912). If the view that the stratum compactum acts
as a girdle, checking undue distension of the intestine (Baecker, 1940), be
accepted, then the intestines of Rutilus and Cyprinus will be more distensible
than that of the carnivorous Gobio since their strata compacta are weaker, a
feature that may be correlated with the more bulky nature of their food.
The muscular coat consists of an inner circular and an outer longitudinal
layer. A transition from striated to non-striated muscle occurs in the circular
layer immediately caudal to the pyloric sphincter and in a roach 7 cm. long
is complete by 2-2 mm. beyond the choledochal duct. The unstriated fibres
first appear internal to the striated fibres, and the transition is accomplished
gradually, so that, in progressively caudal transverse sections, the striated layer
becomes gradually thinner and the non-striated wider.
Using the common carp as an example of teleosts, Li (1937) described a thin
layer of longitudinal fibres next to the submucosa. Using the same technique
on the Cyprinids now being considered it has not proved possible to demon-
strate a continuous sheet of longitudinal fibres in this position, although in a
few places isolated patches of such fibres were seen. A few points remain to
be dealt with concerning the intestine. The choledochal duct unites with the
pancreatic duct and then immediately opens into the intestinal swelling, not,
as described by McVay and Kaan (1940) in the goldfish, on the summit of a
papilla, but simply between two mucosal folds, their epithelium becoming
continuous with that lining the ducts.
In the rectum the submucosa is richly vascular, and since the mucosal folds
are shallower and broader than in the intestine the sub-epithelial cores are
more extensive. The anal outlet is lined by a stratified epithelium containing
numerous pyriform mucus-secreting ce^ls like those of the skin, from which,
indeed, it is distinguished only by the absence of 'Kolbenzellen' characteristic
of the latter. The circular muscle thickens to form an anal sphincter. In all
the three cyprinids the luminal surface of the epithelium of the intestinal
swelling is commonly indented (Text-fig. 50) so that the surface is lowered
forming a pit-like depression. A central cell extends in a straight line from
the pit to the submucosa, but the cells around it are curved so that they form
collectively a sort of 'nest'. These cells have a more or less uniform breadth,
their nuclei are not compressed, and their cytoplasm stains but feebly; the
cells around the 'nest', however, are much compressed, their nuclei elongated,
and their cytoplasm stains more deeply. These 'nests' of cells also occur in
the second limb of the intestine, though less commonly, while in the third
limb of the intestine and rectum they are rare. Their significance is unknown;
they cannot be homologous with primordial gastric glands because they are
post-pyloric in position.
DISCUSSION
Biologists practically agree that the roach is typically omnivorous, the
gudgeon predominantly carnivorous, and the mirror carp mainly herbivorous;
the small quantity of vegetable material taken in by the gudgeon and of
animal food eaten by the mirror carp merely serving to 'balance' the diet (cf.
Kyle, 1926). The following discussion is based on this assumption.
None of the three types possesses teeth on either jaws or palate, but all have
well-developed pharyngeal teeth firmly affixed to the modified fifth gill arch
which oppose a horny pad carried on a special masticatory process of the basi-
occipital. Mastication is thus effected in the pharyngeal region, as it is in
scarids and labrids which crush respectively coral and molluscan shells, and
hence does not obviously interfere with respiration since it takes place posterior
to the respiratory part of the gill apparatus.
The form of the teeth also shows a correlation with the type of diet. Thus
the carnivorous Gobio has biserial hooked teeth, the omnivorous Rutilus has
uniserial teeth, some of which are hooked, while the herbivorous Cyprinus
has three rows of teeth converging towards each other forming a stud-like
'molariform' prominence. Both the relative overall size of the pharyngeal
jaws as well as of the muscles which actuate them are best developed in
Cyprinus and least in Gobio, while the hardness of the horny pad is also in
direct relationship to the amount of plant food ingested.
Of the sixty-odd species of teleosts previously examined and described
(Al-Hussaini, 19476), most of the herbivorous species have serrated, 'incisi-
form' oral teeth and very weak pharyngeal ones. They are thus capable of
nibbling the plants by means of their front teeth and the food enters the mouth
in a ready-macerated form. In the grey mullets and also, according to Wier
and Churchill (1945), in the gizzard shad (Dorosoma cepedianum), the pylorus
forms a 'gizzard' which triturates diatoms and the like. Fishes living on plant
food or hard food have thus acquired one mechanism or another which
enables them to mince their food in preparation for digestion; therefore
the correlation of the morphological features of the alimentary tract with the
feeding habits is complicated by the genetical factor. For example, the carni-
vorous Gobio is more closely comparable to the herbivorous Cyprinus than
the latter is to a herbivorous acanthurid like the doctor fish, Acanthuras sohal,
which possesses oral teeth, a stomach, and pyloric caeca. When Gobio and
Cyprinus are compared with each other, however, several significant points
of difference become apparent, as, for example, the stronger 'molariform'
teeth in Cyprinus and the longer intestine. It is consequently not always
possible to draw hard-and-fast lines between the several groups of feeders
based on certain characteristic features, because fishes, during their progres-
sive evolution, have become variously adapted to the conditions surrounding
them, diverging gradually from each other in the process. An excellent example
is afforded by the three herbivorous species Acanthurus sohal, Cyprinus carpio,
and Mugil auratus belonging to three distinct families. The plant food on
which these fishes graze is comminuted by the serrated 'incisiform' oral teeth
in the first, by the pharyngeal teeth in the second, and by the gizzard-like
pylorus in the third species—three different structures, but all, in fact, fulfilling
a similar function. On the other hand, Gobio can be compared with Mulloides
and Cyprinus with Mugil. The first two are carnivores and the last two are
herbivores, but all four are bottom-feeders, stirring up the mud and seeking
their food from it, and all lose their oral teeth.
Although the cyprinid gut is simple and its relative length (cf. p. 121)
is smaller in Rutilus and Cyprinus than for the average omnivorous or
herbivorous fish, yet estimations of the mucosal area (made here for the
first time) show that this is not small relative to that of mammals, and
that variations in the relative length of the gut may well be compensated
by variations in the mucosal area (cf. p. 123 for a fuller discussion of these
matters).
Turning now to histological features we find that the abundance of taste-
buds is rather to be correlated with the way in which the fish secures its food
than with its nature. Thus when a fish has to select its food from mud {Gobio
and Cyprinus) or sand {Mulloides), or to single out living coral from amongst
inorganic material {Scarus), an efficient gustatory sense is imperative, especially
around the entrance to the mouth cavity, and does not depend on the nature
of the nutritional substances: and taste-buds are much more numerous in
the species named than in the free-feeding, omnivorous Rutilus or the
plankton-feeder Aiherina. Nevertheless, taste-buds are quite common
structures within the mouth in Rutilus.
The histology of the teleostean intestine is one of the simplest among
vertebrates. In the Cyprinids under consideration the intestinal epithelium
shows no special features beyond the formation of the special cellular 'nests'
referred to above (p. 134); indeed, multicellular glands are characteristically
absent from the teleostean intestine except in some of the Gadidae (Jacobs-
hagen, 1937). A spiral value is present in Chirocentrus, while vestiges of it
remain in some of the Salmonidae aqd in Gymnarchus (Goodrich, 1909);
the typhlosole-like structure found in Scarus may well be peculiar to this
genus (Al-Hussaini, 19476). A rectal gland is never present in teleosts but
pyloric caeca frequently are (cf. Al-Hussaini, 1946 and 1947, for a fuller discus-
sion of these structures).
ACKNOWLEDGEMENTS
The writer wishes to acknowledge his great indebtedness and gratitude to
Dr. E. T. B. Francis for his continuous help and invaluable advice, both during
the course of the investigation and in preparing the manuscript. He is also
indebted to Professor L. E. S. Eastham for his encouragement and for extend-
ing the facilities of his Department during his stay in the University of Shef-
field. Thanks are also due to Dr. H. A. F. Gohar, Mar. Biol. Station, Ghardaqa,
Mr. F. S. Russell, F.R.S., Director of the Plymouth Marine Biological Station,
and Professor J. Gray, F.R.S., of Cambridge University for extending facilities
for study in their laboratories, and to Mr. J. Noel Wood, General ManageV
of the Sheffield Corporation Water Works for constant help in supplying
fish from the reservoirs under his control. The writer is also indebted to
Mr. J. Hancock, Senior Laboratory Technician in this Department, for all
the photomicrographs.
SUMMARY
1. The mouth is larger and more protrusible in Gobio and Cyprinus than
in Rutilus, features which may be associated with the mud-grubbing, bottom-
feeding habits of the two former fish, while the arrangement of the adductor
muscles in Rutilus enable it to close its mouth more quickly than they and
hence it can rapidly snap up its free-moving prey.
2. The selection of food is largely by taste in Gobio and Cyprinus, and hence
both are richly supplied with taste-buds from lips to oesophagus, special
concentrations being present on barbs around the mouth. Rutilus, on the
other hand, augments taste by sight. Taste-buds are accordingly more
restricted in distribution and less abundant where they do occur. They are
fewer on the lips; there are no barbs.
3. The relative development of the pharyngeal masticatory apparatus
(horny pad, pharyngeal teeth) bears a direct relationship to the amount of
plant food in the diet, i.e. it increases in the order Gobio, Rutilus, Cyprinus.
4. The mucus-secreting cells attain their maximum development in the
pharynx in all three fishes, as is usual amongst teleosts (cf. Al-Hussaini,
1947a, p. 278) and are thus effectively placed to lubricate the food, irrespective
of its nature, at the very commencement of its journey through the gut.
5. Gill-rakers carrying taste-buds and mucus-secreting glands are present
in all three fish, but they are exceptionally short in Gobio for a bottom-feeding
fish. This may be compensated for to some extent by a pair of food-selecting
palatal cushions.
6. All three fishes are stomachless, the short oesophagus joining the
pharynx directly to the pyloric sphincter. The loss of the food-holding capacity
of the stomach is compensated for by the swelling of the first limb of the
intestine.
7. The intestinal tube is longest and its looping most complex in Cyprinus,
and shortest and with the simplest looping in Gobio. Four parts are recognized
in the intestinal tube, not by external features, but by their mucosal foldings
and certain histological characters.
8. An estimation of the mucosal area shows that the absorptive area of the
intestinal epithelium is practically equal in the three species when related
to the weight of the fish. This ratio has here been called the 'mucosal
coefficient'.
9. The intestinal epithelium comprises two principal histological cell types,
viz. the absorptive cell and the goblet cell.
10. The internal surface across which food substances pass from the cells
to the tissue fluids is greater in Cyprinus and Rutilus than in Gobio, owing to
the greater length of the absorptive cells.
11. In order to be valid, estimations of the relative efficiency of the fish
intestine should take into account the relative length of the gut (R.L.G.), the
mucosal coefficient (Q.M.), and the length of the absorptive cells.
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1947a. Ibid., 80, 251.
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BAECKER, R., 1940. Z. mikr. anat. Forsch., Leipzig, 47, 49.
BAKER, J. R., 1944. Quart. J. micr. Sci.* 85, 1.
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CHU, Y. T., 1935. Biol. Bull. St. John's Univ. Shanghai, 2, 1.
CLARK, W. E. LE GROS, 1945. The Tissues of the Body. Oxford (University Press).
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CURRY, E., 1939. J. Morph., 65, 53.
DAWES, B., 1929. Quart. J. micr. Sci., 73, 243.
DAY, F., 1880-4. The Fishes of Great Britain and Ireland. London (Williams & Norgate).
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1943. Ibid., 72, 183.
EDINGER, L., 1877. Arch. mikr. Anat., 13, 651.
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(A. & C. Black).
1930. The Structure and Development of Vertebrates. London (Macmillan).
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GREVE, 1897. Quoted from Klust.
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JACOBSHAGEN, E., 1911. Jenaische Z. Natw., 47, 525.
1913. Ibid., 49, 373.
1915. Ibid., 53.445-
1937. Handb. d. vergl. Anat. d. Wirbeltiere, ed. by Bolk. Berlin & Wien. Bd. I l l ,
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EXPLANATION OF PLATES
PLATE I
Fig. 1. R. rutilus, showing mucosal folds of roof of mouth, pharynx, oesophagus, and in-
testinal swelling.
Fig. 2. Transverse section of the buccal cavity of Cyprinus carpio. X 22. Note the abun-
dance of taste-buds (T.B.) all over the cavity except on the dorsal surface of the maxillary
valve (MX.V.).
Fig. 3. Tangential section of the lower lip of Cyprinus carpio, showing scores of taste-buds
in cross-section. X85.
Fig. 4. Transverse section of the epithelium lining the lateral part of the roof of the anterior
pharynx of Cyprinus carpio. x 190.
PLATE II
Fig. 5. Transverse section of the anterior pharyngeal region of Cyprinus carpio. x 26.
Fig. 6. Transverse section of the anterior pharynx of Cyprinus carpio passing through a
gill arch. X45.
Fig. 7. Pharyngeal 'jaws' of the three Cyprinids. X2approx. (a) the left 'jaw' of R. rutilus
showing six teeth, medioventral aspect; (6) both 'jaws' of R. rutilus from the dorsal aspect;
note asymmetry of teeth; (c) the right 'jaw' from the same specimen as (a), medioventral
aspect; (rf) the left 'jaw' of Cyprinus carpio, lateral aspect; (e) the right 'jaw' from the same
specimen as the previous one, lateral aspect; (/) both 'jaws' of G. gobio, ventral aspect. In
(a), (b), (c), and (/) the anterior end is pointing downwards.
PLATE III
Fig. 8. Transverse section of the horny pad of R, rutilus. X 70. (a) drawing to show the
cellular types composing the three zones of the pad.
Fig. 9. Transverse section through oesophagus (ES.) & intestinal swelling (l.s.) of R. rutilus.
X2O.
Figs. 2-6, 8, and 9 untouched photomicrographs; figs. 2-6 and 9, fixed Boling's fluid
stained H & E; fig. 8, fixed Boling's fluid, stained Mallory's triple.
LIST OF ABBREVIATIONS USED

D IN THE ILLUSTRATIONS
A.B. air-bladder. M.P. masticatory process of basi-occipital.
A.PH. anterior pharynx. M.S.C. mucus-secreting cells.
AN. angular. M.Z. middle zone.
AR. articular. MD.AD. mandibular portion of adductor
B.C. buccal cavity. mandibulae.
B.M. body musculature. MX. maxilla.
B.Z. basal zone. MX.AD. maxillary portion of adductor mandi-
C.A. coeliaco-mesenteric artery. bulae.
D.A. dorsal aorta. MX.V. maxillary valve.
D.o. dilator operculi. OP. opercular.
DT. dentary. P.D. pneumatic duct.
ES. oesophagus. P.PH.. posterior pharynx.
GH. geniohyoideus. PH.C. pharyngeal cavity.
G.R. gill raker. PL. palatine.
H.P. horny pad. PMX. premaxilla.
l.s. intestinal swelling. POP. preopercular.
IM. intermandibularis. R.A.B.D. retractor arcus branchialis dorsalis.
IN. intestine. R.L. rostral ligament.
I.O. interopercular. s.z. superficial zone.
L. ligament between maxilla, pre- SH. stemohyoideus.
maxilla, and dentary. SOP. subopercular.
L.A.P. levator arcus palatini. ST.M.F. striated muscle-fibre.
LV. liver (hepatopancreas). T.B. taste-bud.
M.c. muscularis circularis (forming T.P. tunica propria.
sphincter). TH.G. thymus gland.
M.L. muscularis longitudinalis. TZ. trapezius.

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109

On the Functional Morphology of the Alimentary Tract

With Three Plates

MATERIAL AND METHODS

THE ANATOMY OF THE ALIMENTARY TRACT

The Pharyngeal Dental Apparatus

The Intestinal Tube

The Surface Area of the Intestinal Mucosa

THE HISTOLOGY OF THE ALIMENTARY TRACT

The Buccal Cavity

TEXT-FIG. 3. Constituent cells of the stratified epithelium of the bucco-pharynx of

TEXT-FIG. 5. Schematized drawings of individual mucosal folds from various parts of

columnar epithelium as the crest of the fold is approached (Text-fig. 5^).

LIST OF ABBREVIATIONS USED

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